The magnetite-based receptors in the beak of birds and their role in avian navigation

Journal of Comparative Physiology A: Neuroethology, Sensory, Neural, and Behavioral Physiology

Volumn 199, Issue 2, 2013, Pages 89-98

  Wiltschko, R ^a   Wiltschko, W ^a  

^a GOETHE UNIVERSITY   (Germany)

Author keywords

'Fixed direction' responses; Magnetic 'map' component; Magnetite based receptors; Pulse treatment; Trigeminal nerve

Indexed keywords

EID: 84872826087     PISSN: 03407594     EISSN: 14321351     Source Type: Journal    
DOI: 10.1007/s00359-012-0769-3     Document Type: Review

References (74)

1. Beason RC, Brennan WJ (1986) Natural and induced magnetization in the Bobolink Dolichonyx oryzivorus (Aves: Icteridae). J Exp Biol 125: 49-56.
2. Beason RC, Nichols JE (1984) Magnetic orientation and magnetically sensitive material in a transequatorial migratory bird. Nature 309: 151-153.
3. Beason RC, Semm P (1987) Magnetic responses of the trigeminal nerve system of the Bobolink (Dolichonyx oryzivorus). Neurosci Lett 80: 229-234.
4. Beason RC, Semm P (1991) Two different magnetic systems in avian orientation. In: Bell BD, Cossee RO, Flux JEC, Heather BD, Hitchmough RA, Robertson CJR, Williams MJ (eds) Acta XX Congr Int Ornithol. New Zealand Ornithol Congr Trust Board, Wellington, pp 1813-1819.
5. Beason RC, Semm P (1996) Does the avian ophthalmic nerve carry magnetic information? J Exp Biol 199: 1241-1244.
6. Beason RC, Dussourd N, Deutschlander M (1995) Behavioral evidence for the use of magnetic material in magnetoreception by a migratory bird. J Exp Biol 198: 141-146.
7. Beason RC, Wiltschko R, Wiltschko W (1997) Pigeon homing: effect of magnetic pulses on initial orientation. Auk 114: 405-415.
8. Blakemore RP (1975) Magnetotactic bacteria. Science 19: 377-379.
9. Brassart J, Kirschvink JL, Philipps JB, Borland SC (1999) Ferromagnetic material in the eastern red-spotted newt Nothophthalmus visidescens. J Exp Biol 202: 3155-3160.
10. Davila AF, Fleissner G, Winklhofer M, Peterson N (2003) A new model for a magnetoreceptor in homing pigeons based on interacting clusters of superparamagnetic magnetite. Phys Chem Earth 28: 647-652.
11. Davila AF, Winklhofer M, Shcherbakov VP, Peterson N (2005) Magnetic pulse affects a putative magnetoreceptor mechanism. Biophys J 89: 56-63.
12. Deutschlander M, Phillips JB, Munro U (2012) Age-dependent orientation of magnetically-simulated geographic displacement in migratory Australian Silvereyes (Zosterops l. lateralis). Wilson J Ornithol 124: 457-477.
13. Diebel CE, Priksch R, Green CR, Nelson P, Walker MM (2000) Magnetite defines a vertebrate magnetoreceptor. Nature 406: 229-301.
14. Eder SHK, Cadiou H, Muhamad A, McNaughton PA, Kirschvink JL, Winklhofer M (2012) Magnetic characterization of isolated candidate vertebrate magnetoreceptor cells. Proc Natl Acad Sci USA 109: 12022-12027.
15. Falkenberg G, Fleissner G, Schuchardt K, Kuehbacher M, Thalau P, Mouritsen H, Heyers D, Wellenreuther G, Fleissner G (2010) Avian magnetoreception: elaborate iron mineral containing dendrites in the upper beak seem to be a common feature of birds. PLoS ONE 5: e9231.
16. Fleissner G, Holtkamp-Rötzler Hanzlik M, Winklhofer M, Fleissner G, Petersen N, Wiltschko W (2003) Ultrastructural analysis of a putative magnetoreceptor in the beak of homing pigeons. J Comp Neurol 458: 350-360.
17. Fleissner G, Stahl B, Thalau P, Falkenberg G, Fleissner G (2007) A novel concept of Fe-mineral-based magnetoreception: histological and physicochemical data from the upper beak of homing pigeons. Naturwissenschaften 94: 631-642.
18. Freire R, Eastwood MA, Joyce M (2011) Minor beak trimming in chickens leads to loss of mechanoreception and magnetoreception. J Anim Sci 89: 1201-1206.
19. Freire R, Dunston E, Fowler EM, McKenzie GL, Quinn CT, Michelsen J (2012) Conditioned response to a magnetic anomaly in the Pekin Duck (Anas platyrhynchos domestica) involves the trigeminal nerve. J Exp Biol 215: 2399-2404.
20. Gagliardo A, Ioalè P, Savini M, Wild M (2008) Navigational abilities of homing pigeons deprived of olfactory or trigeminally mediated magnetic information when young. J Exp Biol 211: 2046-2051.
21. Gagliardo A, Ioalè P, Savini M, Wild M (2009) Navigational abilities of adult and experienced homing pigeons deprived of olfactory or trigeminally mediated magnetic information. J Exp Biol 212: 3119-3124.
22. Hanzlik M, Heunemann C, Holtzkamp-Rötzler E, Winklhofer M, Petersen N, Fleissner G (2000) Superparamagnetic magnetite in the upper beak of homing pigeons. Biometals 13: 325-331.
23. Hellinger J, Hoffmann K-P (2012) Magnetic field perception in the rainbow trout Oncyrynchus mykiss: magnetite mediated, light dependent or both? J Comp Physiol 198: 593-605.
24. Heyers D, Zapka M, Hoffmeister M, Wild JM, Mouritsen H (2010) Magnetic field changes activate the trigeminal brainstem complex in a migratory bird. Proc Natl Acad Sci USA 107: 9394-9399.
25. Holland RA (2010) Differential effects of magnetic pulses on the orientation of naturally migrating birds. J R Soc Interface 7: 1617-1625.
26. Holland RA, Helm B (2012) The effect of strong magnetic pulses on the behavior on naturally migrating songbirds. Abstract, 6th Eur Conf Behav Biol, Essen.
27. Holland RA, Thorup K, Gagliardo A, Bisson IA, Knecht E, Mizrahi D, Wikelski (2009) Testign the role of sensory systems in the migratory heading of a songbird. J Exp Biol 212: 4065-4071.
28. Keeton WT (1971) Magnets interfere with pigeon homing. Proc Natl Acad Sci USA 68: 102-106.
29. Keeton WT, Larkin TS, Windsor DM (1974) Normal fluctuations in the earth's magnetic field influence pigeon orientation. J Comp Physiol 95: 95-103.
30. Kirschvink JL, Gould JL (1981) Biogenetic magnetite as a basis for magnetic field detection in animals. BioSystems 13: 181-201.
31. Kirschvink JL, Walker MM (1985) Particle-size considerations for magnetite-based magnetoreceptors. In: Kirschvink JL, Jones DS, MacFadden BJ (eds) Magnetite biomineralization and magnetoreception in organisms. Plenum Press, New York, pp 243-256.
32. Kirschvink JL, Jones DS, MacFadden BJ (eds) (1985a) Magnetite biomineralization and magnetoreception in organisms. Plenum Press, New York.
33. Kirschvink JL, Walker MM, Chang S-B, Dizon AE, Peterson KA (1985b) Chains of single-domain magnetite particles in Chinook salmon, Oncyrhynchus tshawytscha. J Comp Physiol A 157: 375-381.
34. Lowenstam HA (1962) Magnetite in denticle capping in recent chitons (Polyplacophora). Geol Soc Am Bull 73: 435-438.
35. Mann S, Sparks HCH, Walker MM, Kirschvink JL (1988) Ultrastructure, morphology and organization of biogenic magnetite from Sockeye Salmon, Oncyrhynchus nerka: implications for magnetoreception. J Exp Biol 140: 35-49.
36. Mora CV, Davison M, Wild JM, Walker MM (2004) Magnetoreception and its trigeminal mediation on the homing pigeons. Nature 432: 508-511.
37. Munro U, Munro JA, Phillips JB, Wiltschko R, Wiltschko W (1997) Evidence for a magnetite-based navigational 'map' in birds. Naturwissenschaften 84: 26-28.
38. Ritz T (2011) Quantum effects in biology: bird navigation. Procedia Chem 3: 262-275.
39. Ritz T, Adem S, Schulten K (2000) A model for photoreceptor-based magnetorecption in birds. Biophys J 78: 707-718.
40. Ritz T, Thalau P, Phillips JB, Wiltschko R, Wiltschko W (2004) Resonance effects indicate a radical-pair mechanism for avian magnetic compass. Nature 429: 177-180.
41. Ritz T, Ahmad M, Mouritsen H, Wiltschko R, Wiltschko W (2010) Photoreceptor-based magneto-receptiom: optimal design of receptor molecules, cells, and neural processing. J R Soc Interface 7 Focus 2: S135-S146.
42. Schiffner I, Wiltschko R (2011) Temporal fluctuation of the geomagnetic field affect pigeons' entire homing flight. J Comp Physiol A 197: 765-772.
43. Semm P, Beason RC (1990) Responses to small magnetic variations by the trigeminal system of the bobolink. Brain Res Bull 25: 735-740.
44. Shcherbakov VP, Winklhofer (1999) The osmotic magnetometer: a new model for magnetite-based magnetoreceptors in animals. Eur Biophys J 28: 380-392.
45. Solovyov IA, Greiner W (2007) Theoretical analysis of an iron-mineral-based magnetoreceptor model in birds. Biophys J 93: 1493-1509.
46. Stapput K, Thalau P, Wiltschko R, Wiltschko W (2008) Orientation of birds in total darkness. Curr Biol 18: 602-606.
47. Tian L, Xiao B, Lin W, Zhang S, Zhu R, Pan Y (2007) Testing for the presence of magnetite in the upper-beak skin of homing pigeons. Biometals 20: 197-203.
48. Tian L, Lin W, Zhang S, Pan Y (2010) Bat head contains soft magnetic particles: evidence from magnetism. Bioelectromagnetics 31: 499-503.
49. Treiber CD, Salzer MC, Riegler J, Edelmann N, Sugar C, Breuss M, Pichler P, Cadiou H, Saunders M, Shaw J, Keays DA (2012) Clusters of iron-rich cells in the upper beak of pigeons are macrophages not magnetosensitive neurons. Nature 484: 367-370.
50. Walcott C (1978) Anomalies in the earth's magnetic field increase the scatter of pigeons' vanishing bearings. In: Schmidt-Koenig K, Keeton WT (eds) Animal migration, navigation, and homing. Springer, Berlin, Heidelberg, New York, pp 143-151.
51. Walcott C, Gould JL, Kirschvink JL (1979) Pigeons have magnets. Science 205: 1027-1029.
52. Walker MM (2008) A model for encoding magnetic-field intensity by magnetite based magnetoreceptor cells. J Theor Biol 250: 85-91.
53. Walker MM, Diebel CE, Haugh CV, Pankhurst PM, Montgomery JC, Green CR (1997) Structure and function of the vertebrate magnetic sense. Nature 390: 371-376.
54. Wegner R, Begall S, Burda H (2006) Magnetic compass in the cornea: local anesthesia impairs orientation in a mammal. J Exp Biol 209: 4747-4750.
55. Williams MN, Wild JM (2001) Trigeminally innervated iron-containing structures in the beak of homing pigeons, and other birds. Brain Res 889: 243-246.
56. Wiltschko W (1968) Über den Einfluß statischer Magnetfelder auf die Zugorientierung der Rotkehlchen (Erithacus rubecula). Z Tierpsychol 25: 536-558.
57. Wiltschko W, Wiltschko (1972) The magnetic compass of European Robins. Science 176: 62-64.
58. Wiltschko W, Munro U, Beason RC, Ford H, Wiltschko R (1994) A magnetic pulse leads to a temporary deflection in the orientation of migratory birds. Experientia 50: 697-700.
59. Wiltschko W, Munro U, Ford H, Wiltschko R (1998) Effect of a magnetic pulse on the orientation of Silvereyes, Zosterops l. lateralis, during spring migration. J Exp Biol 201: 3257-3261.
60. Wiltschko W, Munro U, Wiltschko R, Kirschvink J (2002) Magnetite-based magnetoreception in birds: the effect of a biasing field and a pulse on migratory behavior. J Exp Bio 20: 3031-3037.
61. Wiltschko W, Munro U, Ford H, Wiltschko R (2006) Bird navigation: what type of information does the magnetite-based receptor provide? Proc R Soc B 273: 2815-2850.
62. Wiltschko R, Stapput K, Ritz T, Thalau P, Wiltschko W (2007) Magnetoreception in birds: different physical processes for two types of directional responses. HFSP Journal 1: 41-47.
63. Wiltschko W, Ford H, Munro U, Winklhofer M, Wiltschko R (2007) Magnetite-based magneto-reception: the effect of repeated pulsing on the orientation of migratory birds. J Comp Physiol A 193: 515-522.
64. Wiltschko R, Munro U, Ford H, Stapput K, Wiltschko W (2008) Light-dependent magnetoreception: orientation behaviour of migratory birds under dim red light. J Exp Biol 211: 3344-3350.
65. Wiltschko R, Schiffner I, Wiltschko W (2009) A strong magnetic anomaly affects pigeon navigation. J Exp Biol 212: 2983-2990.
66. Wiltschko W, Munro U, Ford H, Wiltschko R (2009) Avian orientation: the pulse effect is mediated by the magnetite receptors in the upper beak. Proc R Soc B 276: 2227-2232.
67. Wiltschko R, Stapput K, Thalau P, Wiltschko W (2010a) Directional orientation of birds by the magnetic field under different light conditions. J R Soc Interface 7 Focus 2: S163-S177.
68. Wiltschko R, Schiffner I, Fuhrmann P, Wiltschko W (2010b) The role of the magnetite-based receptors in the beak in pigeon homing. Curr Biol 20: 1534-1538.
69. Wiltschko W, Wiltschko R, Ritz T (2011) The mechanism of the avian magnetic compass. Procedia Chem 3: 276-284.
70. Wiltschko R, Dehe L, Gehring D, Thalau P, Wiltschko W (2012) Interactions between the visual and the magnetoreception system: Different effects of bichromatic light regimes in the directional behavior of migratory birds. J Physiol Paris. http://dx. doi. org/101016/j. jphysparis. 2012. 03. 003.
71. Winklhofer M, Kirschvink JL (2010) A quantitative assessment of torque-transducer models for magnetoreception. J R Soc Interface 7 Focus 2: S273-S289.
72. Winklhofer M, Holtkamp-Rötzler E, Hanzlik M, Fleissner G, Petersen N (2001) Clusters of superparamagentic magnetite particles in the upper-beak skin of homing pigeons: evidence of a magnetoreceptor? Eur J Mineral 13: 659-669.
73. Yorke E (1979) A possible magnetic transducer in birds. J Theor Biol 77: 101-105.
74. Zapka M, Heyers D, Hein CM, Engels S, Schneider N-L, Hans J, Weiler S, Dreyer D, Kishkinev D, Wild JM, Mouritsen H (2009) Visual but not trigeminal mediation of magnetic compass information in a migratory birds. Nature 461: 1274-1278.